Helgol Mar Res (2013) 67:109–120 DOI 10.1007/s10152-012-0308-1 ORIGINAL ARTICLE Nurse egg consumption and intracapsular development in the common whelk Buccinum undatum (Linnaeus 1758) Kathryn E. Smith • Sven Thatje Received: 29 November 2011 / Revised: 12 April 2012 / Accepted: 17 April 2012 / Published online: 3 May 2012 Ó Springer-Verlag and AWI 2012 Abstract Intracapsular development is common in mar- each capsule during development in the common whelk. ine gastropods. In many species, embryos develop along- The initial differences observed in nurse egg uptake may side nurse eggs, which provide nutrition during ontogeny. affect individual predisposition in later life. The common whelk Buccinum undatum is a commercially important North Atlantic shallow-water gastropod. Devel- Keywords Intracapsular development Á Buccinum opment is intracapsular in this species, with individuals undatum Á Nurse egg partitioning Á Competition Á hatching as crawling juveniles. While its reproductive Reproduction cycle has been well documented, further work is necessary to provide a complete description of encapsulated devel- opment. Here, using B. undatum egg masses from the south Introduction coast of England intracapsular development at 6 °Cis described. Number of eggs, veligers and juveniles per Many marine gastropods undergo intracapsular development capsule are compared, and nurse egg partitioning, timing of inside egg capsules (Thorson 1950; Natarajan 1957;D’Asaro nurse egg consumption and intracapsular size differences 1970; Fretter and Graham 1985). Embryos develop within the through development are discussed. Total development protective walls of a capsule that safeguards against factors took between 133 and 140 days, over which 7 ontogenetic such as physical stress, predation, infection and salinity stages were identified. The number of both eggs and veli- changes (Thorson 1950;Pechenik1983, 1999; Strathmann gers were significantly related to capsule volume, with 1985;Rawlings1995, 1999). Periods of encapsulation vary; approximately 1 % of eggs developing per capsule. Each some species are released as veligers and undergo a plank- early veliger consumed nurse eggs rapidly over just tonic stage before reaching adult life (mixed development), 3–7 days. Within each capsule, initial development was while others display direct development, hatching from cap- asynchronous, but it became synchronous during the veli- sules as crawling juveniles (Natarajan 1957;D’Asaro1970; ger stage. No evidence for cannibalism was found during Pechenik 1979). When direct development occurs, embryos development, but large size differences between embryos are often accompanied in a capsule by nurse eggs, non- developing within each capsule were observed, and occa- developing food eggs, which provide nutrition during devel- sionally ‘empty’ veligers were seen, which had not opment (Thorson 1950;Spight1976b; Rivest 1983;Lahbib successfully consumed any nurse eggs. These results et al. 2010). These are usually indistinguishable from indicate a high level of competition for nurse eggs within embryos in the very early stage of ontogeny and are consumed during development, potentially increasing size of juveniles Communicated by Martin Thiel. at hatching (Thorson 1950). In some species, nutrition may also be provided by intracapsular fluid or protein from capsule K. E. Smith (&) Á S. Thatje walls (Bayne 1968;Sto¨ckmann-Bosbach 1988;Moran1999; Ocean and Earth Science, University of Southampton, Ojeda and Chaparro 2004). National Oceanography Centre, Southampton, European Way, Southampton SO14 3ZH, UK Generally speaking, nurse egg consumption occurs over e-mail: [email protected] a period of several weeks or months. It commences some 123 110 Helgol Mar Res (2013) 67:109–120 weeks into development as embryos form, and nurse eggs embryo size ranges through development. The common are then slowly consumed throughout much of develop- whelk is a scavenger found widespread in coastal areas in the ment (Chaparro and Paschke 1990; Ilano et al. 2004; North Atlantic. It is generally found from the shallow sub- Lahbib et al. 2010). The number of nurse eggs consumed tidal down to a few hundred metres of water depth (Valen- during this period varies across species. Ratios range from tinsson et al. 1999; Valentinsson 2002; Rosenberg 2009), 1.7 nurse eggs per embryo in the Pacific shallow-water with a latitudinal range from 38°Nto79°N spanning the muricid Acanthinucella spirata (Spight 1976a), to between North Atlantic and Arctic Oceans (OBIS http://iobis.org/ 50,000 and 100,000 nurse eggs per embryo in the North mapper/?taxon=Buccinumundatum). Buccinum undatum is Atlantic deep-sea buccinid Volutopsius norwegicus (Thor- an important commercial species, providing locally valuable son 1950). Often, within a species, the nurse egg to embryo fisheries in several areas around the North Atlantic including ratio varies from capsule to capsule within one clutch the UK, the USA and Canada (Hancock 1967; Morel and (Thorson 1950; Spight 1976a). For example, Rivest (1983) Bossy 2004). It has been suggested as a good candidate for found this ratio in the buccinid Lirabuccinum dirum to vary aquaculture (Nasution and Roberts 2004) and globally, from 11 to 46 across capsules. Similar differences have demand for it is continuously increasing (Department of been reported for other gastropods (Natarajan 1957; Spight Marine Resources www.maine.gov/dmr/rm/whelks.html). 1976a). Within a capsule however, there is usually little Its reproductive cycle has been well documented across its variation in the number of nurse eggs ingested by each range (Hancock 1967; Martel et al. 1986a, b; Kideys et al. embryo, with all embryos generally being equal in their 1993; Valentinsson 2002). Females group to deposit small ability to consume. Any differences observed are minimal, creamy coloured spherical egg capsules (Martel et al. and juveniles hatching from each capsule are normally of a 1986a). Each lays approximately 80–150, which collectively very similar size (Natarajan 1957; Spight 1976a; Rivest can create large egg masses of hundreds to thousands of 1983; Chaparro and Paschke 1990; Chaparro et al. 1999; capsules (Fretter and Graham 1985; Valentinsson 2002). The Lloyd and Gosselin 2007). Large size differences amongst time of year for spawning varies in this species across its capsulemates are unusual, but have been reported in some distribution. In coastal waters of the UK, egg capsules are species of muricid gastropod (Gallardo 1979; Gonza´lez and laid during the autumn and winter months (predominantly Gallardo 1999; Cumplido et al. 2011). In gastropods, the late November–January) as annual water temperatures drop number of eggs inside a capsule is usually positively below 9 °C (Hancock 1967; Kideys et al. 1993). In the related to capsule size. Within a species, larger capsules northwest Atlantic, egg laying instead takes place in spring hold more eggs and more developing embryos (Gallardo (late May to mid July) as water temperatures warm 1979; Pechenik et al. 1984; Miloslavich and Dufresne (approximately 2–3 °C) (Martel et al. 1986a). Intracapsular 1994). The relationship between capsule size and number development takes between 2.5 and 9 months across the of eggs (including nurse eggs) has, however, previously species range (Fretter and Graham 1985; Martel et al. 1986a; been shown to be stronger than the relationship between Kideys et al. 1993; Nasution 2003). Given the widespread capsule size and number of developing embryos (Spight distribution of B. undatum, its current commercial impor- 1976b). In some cases, the number of developing embryos tance and its potential as a future candidate for aquaculture, it within a capsule has been found to be independent of is important to understand fully the development in this capsule volume. This suggests that embryos are distributed species. at random, while nurse eggs are regularly placed amongst Here, we examine intracapsular development in B. und- capsules (Rivest 1983; Chaparro et al. 1999). atum using a population from the south coast of England, at Intracapsular development and nurse egg and embryo the southern end of the species distribution. Number of eggs partitioning have been investigated in several species of and number of developing veligers and juveniles are exam- marine gastropod (Natarajan 1957; D’Asaro 1970; Spight ined through development. Ontogenetic stages are described 1976a; Rivest 1983; Cumplido et al. 2011). While some in detail including nurse egg partitioning, nurse egg con- attempts have been made to examine encapsulated devel- sumption and intracapsular ranges in embryo sizes. opment in the common whelk Buccinum undatum (Portmann 1925; Fretter and Graham 1985; Nasution 2003), it has not yet been fully described. Nasution (2003) gives the most in- Materials and methods depth account of development to date, but his descriptions are incomplete and his reports of nurse egg consumption do Embryonic development not match our observations. Descriptions from Portmann (1925) better fit our observations but lack detail. There are In order to study the intracapsular development in also gaps in the current literature, and very limited knowl- B. undatum, 150 adults were collected from Viviers UK in edge exists on nurse egg partitioning and intracapsular late November 2009 (www.fishmarketportsmouth.co.uk). 123 Helgol Mar Res (2013) 67:109–120 111 Adults were originally gathered from the Solent, UK (Southampton, UK, 50°500 N, 001°190 W)